Oxytocin modulates cooperation within and competition between groups: An integrative review and research agenda

Abstract The author reviews evidence that hypothalamic release (or infusion) of the neuropeptide oxytocin modulates the regulation of cooperation and conflict among humans because of three reasons. First, oxytocin enables social categorization of others into in-group versus out-group. Second, oxytocin dampens amygdala activity and enables the development of trust. Third, and finally, oxytocin up-regulates neural circuitries (e.g., inferior frontal gyrus, ventromedial prefrontal cortex, caudate nucleus) involved in empathy and other-concern. Consistent with an evolutionary perspective on the functionality of cooperation, it is concluded that oxytocin-motivated cooperation is mostly parochial—it motivates (i) in-group favoritism, (ii) cooperation towards in-group but not out-group members, and (iii) defense-motivated non-cooperation towards threatening outsiders. Thus, in addition to its well-known role in reproduction and pair–bond formation, oxytocin's primary functions include in-group “tend-and-defend.” This review concludes with avenues for new research on oxytocin's functions in within-group cooperation and between-group competition. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.

[1]  Shaul Shalvi,et al.  The Neuropeptide Oxytocin Regulates Parochial Altruism in Intergroup Conflict Among Humans , 2010, Science.

[2]  P. Shaver,et al.  Boosting Attachment Security to Promote Mental Health, Prosocial Values, and Inter-Group Tolerance , 2007 .

[3]  G. Āllport.  The Nature of Prejudice , 1954 .

[4]  C. Frith,et al.  The role of social cognition in decision making , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  R. Landgraf,et al.  An intrinsic vasopressin system in the olfactory bulb is involved in social recognition , 2010, Nature.

[6]  C. Kirschbaum,et al.  Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress , 2003, Biological Psychiatry.

[7]  P. Zak,et al.  Oxytocin is associated with human trustworthiness , 2005, Hormones and Behavior.

[8]  Madan M. Pillutla,et al.  Unfairness, Anger, and Spite: Emotional Rejections of Ultimatum Offers , 1996 .

[9]  Nir Halevy,et al.  “In-Group Love” and “Out-Group Hate” as Motives for Individual Participation in Intergroup Conflict , 2008, Psychological science.

[10]  Ulrike Ehlert,et al.  Effects of different kinds of couple interaction on cortisol and heart rate responses to stress in women , 2007, Psychoneuroendocrinology.

[11]  A. Colman.  Cooperation, psychological game theory, and limitations of rationality in social interaction , 2003, Behavioral and Brain Sciences.

[12]  Thomas Baumgartner,et al.  Article the Neural Circuitry of a Broken Promise , 2022 .

[13]  E. Phelps.  Emotion and cognition: insights from studies of the human amygdala. , 2006, Annual review of psychology.

[14]  L Cosmides,et al.  Can race be erased? Coalitional computation and social categorization , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Ulrike Ehlert,et al.  Intranasal Oxytocin Increases Positive Communication and Reduces Cortisol Levels During Couple Conflict , 2009, Biological Psychiatry.

[16]  S. Shamay-Tsoory.  The Neural Bases for Empathy , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[17]  A. Douglas,et al.  Brain Oxytocin Correlates with Maternal Aggression: Link to Anxiety , 2005, The Journal of Neuroscience.

[18]  A. A. Lumsdaine,et al.  The American soldier: Combat and its aftermath. (Studies in social psychology in World War II), Vol. 2 , 1949 .

[19]  J. Dovidio,et al.  Prosocial behavior: multilevel perspectives. , 2005, Annual review of psychology.

[20]  T. Schelling.  The Strategy of Conflict , 1963 .

[21]  H. Engeland,et al.  Intranasal oxytocin increases fathers’ observed responsiveness during play with their children: A double-blind within-subject experiment , 2010, Psychoneuroendocrinology.

[22]  C. Zogmaister,et al.  The role of familiarity in implicit memory effects: the case of exemplar activation , 2000 .

[23]  S. Stouffer,et al.  The American soldier : combat and its aftermath , 1949 .

[24]  Gary Bornstein,et al.  Intergroup Conflict: Individual, Group, and Collective Interests , 2003, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[25]  Geoffrey Bird,et al.  Effects of Oxytocin and Prosocial Behavior on Brain Responses to Direct and Vicariously Experienced Pain , 2008, Emotion.

[26]  U. Fischbacher,et al.  Oxytocin Shapes the Neural Circuitry of Trust and Trust Adaptation in Humans , 2008, Neuron.

[27]  E. Ostrom.  A Behavioral Approach to the Rational Choice Theory of Collective Action: Presidential Address, American Political Science Association, 1997 , 1998, American Political Science Review.

[28]  Mark Rotteveel,et al.  Convergent and divergent responses to emotional displays of ingroup and outgroup. , 2011, Emotion.

[29]  S. Fiske.  Interpersonal Stratification: Status, Power, and Subordination , 2010 .

[30]  T. Mappes,et al.  Between-group competition and human cooperation , 2008, Proceedings of the Royal Society B: Biological Sciences.

[31]  J. Pineda,et al.  The role of the left inferior frontal gyrus in social perception: An rTMS study , 2011, Brain Research.

[32]  C. D. De Dreu,et al.  Motivated Information Processing in Group Judgment and Decision Making , 2008, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[33]  Ross A. Hammond,et al.  The Evolution of Ethnocentrism , 2006 .

[34]  Peter A. Bos,et al.  Acute effects of steroid hormones and neuropeptides on human social–emotional behavior: A review of single administration studies , 2012, Frontiers in Neuroendocrinology.

[35]  Raffael Kalisch,et al.  Oxytocin Attenuates Affective Evaluations of Conditioned Faces and Amygdala Activity , 2008, The Journal of Neuroscience.

[36]  J. Holt-Lunstad,et al.  Influence of a “Warm Touch” Support Enhancement Intervention Among Married Couples on Ambulatory Blood Pressure, Oxytocin, Alpha Amylase, and Cortisol , 2008, Psychosomatic medicine.

[37]  Howard Raiffa,et al.  Games and Decisions: Introduction and Critical Survey. , 1958 .

[38]  O. Luminet,et al.  Oxytocin not only increases trust when money is at stake, but also when confidential information is in the balance , 2010, Biological Psychology.

[39]  Michel J. J. Handgraaf,et al.  Oxytocin modulates selection of allies in intergroup conflict , 2012, Proceedings of the Royal Society B: Biological Sciences.

[40]  Larry J. Young,et al.  Neuropeptidergic regulation of affiliative behavior and social bonding in animals , 2006, Hormones and Behavior.

[41]  Peter Klaver,et al.  Oxytocin Makes a Face in Memory Familiar , 2009, The Journal of Neuroscience.

[42]  Olivier Corneille,et al.  Oxytocin Makes People Trusting, Not Gullible , 2010, Psychological science.

[43]  William A. Cunningham,et al.  The Quadruple Process model approach to examining the neural underpinnings of prejudice , 2008, NeuroImage.

[44]  Michel J. J. Handgraaf,et al.  Reply to Chen et al.: Perhaps goodwill is unlimited but oxytocin-induced goodwill is not , 2011, Proceedings of the National Academy of Sciences.

[45]  Angela Sirigu,et al.  Promoting social behavior with oxytocin in high-functioning autism spectrum disorders , 2010, Proceedings of the National Academy of Sciences.

[46]  Clyde H. Coombs,et al.  A reparameterization of the prisoner's dilemma game , 1973 .

[47]  John A Updegraff,et al.  Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. , 2000, Psychological review.

[48]  P. Zak,et al.  Oxytocin Increases Generosity in Humans , 2007, PloS one.

[49]  Henrik Walter,et al.  Functional relations of empathy and mentalizing: An fMRI study on the neural basis of cognitive empathy , 2011, NeuroImage.

[50]  I. Neumann.  Brain Oxytocin: A Key Regulator of Emotional and Social Behaviours in Both Females and Males , 2008, Journal of neuroendocrinology.

[51]  Maarten A. S. Boksem,et al.  Oxytocin Modulates Amygdala, Insula, and Inferior Frontal Gyrus Responses to Infant Crying: A Randomized Controlled Trial , 2011, Biological Psychiatry.

[52]  Jeffrey T. Polzer,et al.  Intergroup Negotiations , 1996 .

[53]  A. Tobeña.  Lethal Altruists , 2009, Annals of the New York Academy of Sciences.

[54]  Jamil Zaki,et al.  Oxytocin Selectively Improves Empathic Accuracy , 2010, Psychological science.

[55]  M. Brewer.  The Psychology of Prejudice: Ingroup Love and Outgroup Hate? , 1999 .

[56]  M. Deutsch.  The Resolution of ConflictConstructive and Destructive Processes , 1974 .

[57]  Joyce E. Berg,et al.  Trust, Reciprocity, and Social History , 1995 .

[58]  S. Kéri,et al.  Oxytocin response in a trust game and habituation of arousal , 2011, Physiology & Behavior.

[59]  Roderick M. Kramer,et al.  Choice behavior in social dilemmas: Effects of social identity, group size, and decision framing. , 1986 .

[60]  R. Dawes,et al.  A Conceptual Review of Decision Making in Social Dilemmas: Applying a Logic of Appropriateness , 2004, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[61]  Holly Arrow.  The Sharp End of Altruism , 2007, Science.

[62]  J. Rilling,et al.  The neuroscience of social decision-making. , 2011, Annual review of psychology.

[63]  M. Kavaliers,et al.  Sociality, Pathogen Avoidance, and the Neuropeptides Oxytocin and Arginine Vasopressin , 2011, Psychological science.

[64]  P. Brennan,et al.  Mammalian social odours: attraction and individual recognition , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[65]  A. Manstead,et al.  An interpersonal approach to emotion in social decision making: the emotions as social information model , 2010 .

[66]  W. Young,et al.  Oxytocin and the oxytocin receptor underlie intrastrain, but not interstrain, social recognition , 2009, Genes, brain, and behavior.

[67]  R. D. Alexander,et al.  The evolution of social behavior , 1974 .

[68]  J. Mateo.  Recognition systems and biological organization: The perception component of social recognition , 2004 .

[69]  A. Guastella,et al.  Acute effects of intranasal oxytocin on subjective and behavioral responses to social rejection. , 2010, Experimental and clinical psychopharmacology.

[70]  S. Komorita,et al.  Interpersonal Relations: Mixed-Motive Interaction , 1995 .

[71]  K. Uvnäs‐Moberg,et al.  OXYTOCIN MAY MEDIATE THE BENEFITS OF POSITIVE SOCIAL INTERACTION AND EMOTIONS 1 The purpose of this paper is to describe the neuroendocrine mechanisms of positive social interactions. 1 , 1998, Psychoneuroendocrinology.

[72]  I. Penton-Voak,et al.  Oxytocin and social perception: Oxytocin increases perceived facial trustworthiness and attractiveness , 2009, Hormones and Behavior.

[73]  Terence C. Burnham,et al.  Engineering altruism: a theoretical and experimental investigation of anonymity and gift giving , 2003 .

[74]  Jonathan P. Beauchamp,et al.  No Association between Oxytocin Receptor (OXTR) Gene Polymorphisms and Experimentally Elicited Social Preferences , 2010, PloS one.

[75]  K. W. Carsten,et al.  Social conflict: the emergence and consequences of struggle and negotiation , 2010 .

[76]  David De Cremer,et al.  Social value orientations and the strategic use of fairness in ultimatum bargaining , 2004 .

[77]  Peter J. Richerson,et al.  Cultural transmission and the evolution of cooperative behavior , 1982 .

[78]  S. Herpertz,et al.  Oxytocin Improves “Mind-Reading” in Humans , 2007, Biological Psychiatry.

[79]  G. Rizzolatti,et al.  A unifying view of the basis of social cognition , 2004, Trends in Cognitive Sciences.

[80]  K. Preuschoff,et al.  Neural Responses to Ingroup and Outgroup Members' Suffering Predict Individual Differences in Costly Helping , 2010, Neuron.

[81]  Gareth Leng,et al.  Dendritic peptide release and peptide-dependent behaviours , 2006, Nature Reviews Neuroscience.

[82]  Toshio Yamagishi,et al.  False friends are worse than bitter enemies: “Altruistic” punishment of in-group members , 2004 .

[83]  Thomas R. Insel,et al.  Social amnesia in mice lacking the oxytocin gene , 2000, Nature Genetics.

[84]  N. Kerr,et al.  "Me versus just us versus us all" categorization and cooperation in nested social dilemmas. , 2002, Journal of personality and social psychology.

[85]  Michael G Ruscio,et al.  Oxytocin, vasopressin and sociality. , 2008, Progress in brain research.

[86]  L. Young,et al.  Erratum to “Neuropeptidergic regulation of affiliative behavior and social bonding in animals” [Horm. Behav. 50 (2006) 506–517] , 2007, Hormones and Behavior.

[87]  A. Kruglanski,et al.  Fully Committed: Suicide Bombers' Motivation and the Quest for Personal Significance , 2009 .

[88]  Michael X. Cohen,et al.  Oxytocin Enhances Amygdala-Dependent, Socially Reinforced Learning and Emotional Empathy in Humans , 2010, The Journal of Neuroscience.

[89]  Zuleyma Tang-Martinez,et al.  The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation , 2001, Behavioural Processes.

[90]  Frances S. Chen,et al.  Oxytocin and intergroup relations: Goodwill is not a fixed pie , 2011, Proceedings of the National Academy of Sciences.

[91]  J. Decety,et al.  Neural correlates of feeling sympathy , 2003, Neuropsychologia.

[92]  S. Fiske.  What We Know Now About Bias and Intergroup Conflict, the Problem of the Century , 2002 .

[93]  Samuel Bowles,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 and S2 Table S1 References and Notes the Coevolution of Parochial Altruism and War , 2022 .

[94]  Giuseppe Pagnoni,et al.  Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men , 2012, Psychoneuroendocrinology.

[95]  B. Frey,et al.  Social Distance and Other-Regarding Behavior in Dictator Games: Comment , 1999 .

[96]  Carolyn H. Declerck,et al.  Oxytocin and cooperation under conditions of uncertainty: The modulating role of incentives and social information , 2010, Hormones and Behavior.

[97]  Markus Heinrichs,et al.  Oxytocin, vasopressin, and human social behavior , 2009, Frontiers in Neuroendocrinology.

[98]  Larry J. Young,et al.  Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior , 2009, Frontiers in Neuroendocrinology.

[99]  S. Shamay-Tsoory,et al.  The effect of intranasal administration of oxytocin on fear recognition , 2010, Neuropsychologia.

[100]  A. Todorov,et al.  The functional basis of face evaluation , 2008, Proceedings of the National Academy of Sciences.

[101]  Peter Kirsch,et al.  Oxytocin Modulates Neural Circuitry for Social Cognition and Fear in Humans , 2005, The Journal of Neuroscience.

[102]  Riitta Hari,et al.  Competing with peers: Mentalizing-related brain activity reflects what is at stake , 2009, NeuroImage.

[103]  Michel J. J. Handgraaf,et al.  People avoid situations that enable them to deceive others , 2011 .

[104]  W. Hamilton,et al.  The Evolution of Cooperation , 1984 .

[105]  Oliver P. John,et al.  Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans , 2009, Proceedings of the National Academy of Sciences.

[106]  C. D. De Dreu,et al.  Influence of social motives on integrative negotiation: a meta-analytic review and test of two theories. , 2000, Journal of personality and social psychology.

[107]  Thomas R. Insel,et al.  The Neuroendocrine Basis of Social Recognition , 2002, Frontiers in Neuroendocrinology.

[108]  R. Sapolsky,et al.  Disruption of Fear Memory Through Dual-Hormone Gene Therapy , 2009, Biological Psychiatry.

[109]  Ilanit Gordon,et al.  Prolactin, Oxytocin, and the development of paternal behavior across the first six months of fatherhood , 2010, Hormones and Behavior.

[110]  D. G. Pruitt,et al.  NEGOTIATION AND MEDIATION , 1992 .

[111]  Eliot R. Smith,et al.  On the automatic evaluation of social exemplars. , 2004, Journal of personality and social psychology.

[112]  T. Clutton‐Brock,et al.  Experimental peripheral administration of oxytocin elevates a suite of cooperative behaviours in a wild social mammal , 2011, Proceedings of the Royal Society B: Biological Sciences.

[113]  J. G. Holmes,et al.  The role of situational restrictiveness on self-fulfilling prophecies: A theoretical and empirical extension of Kelley and Stahelski's triangle hypothesis. , 1975 .

[114]  Melvin J. Kimmel,et al.  Twenty Years of Experimental Gaming: Critique,Synthesis, and Suggestions for the Future , 1977 .

[115]  Colin Camerer,et al.  Not So Different After All: A Cross-Discipline View Of Trust , 1998 .

[116]  J. Bowlby.  Attachment and loss: retrospect and prospect. , 1969, The American journal of orthopsychiatry.

[117]  Xiaolin Zhou,et al.  Social distance modulates recipient's fairness consideration in the dictator game: An ERP study , 2011, Biological Psychology.

[118]  B. Averbeck,et al.  Oxytocin Decreases Aversion to Angry Faces in an Associative Learning Task , 2010, Neuropsychopharmacology.

[119]  Zoe R. Donaldson,et al.  Oxytocin, Vasopressin, and the Neurogenetics of Sociality , 2008, Science.

[120]  Ernst Fehr,et al.  Parochial altruism in humans , 2006, Nature.

[121]  S. Fiske,et al.  Social groups that elicit disgust are differentially processed in mPFC. , 2007, Social cognitive and affective neuroscience.

[122]  E. Fehr,et al.  Altruistic punishment in humans , 2002, Nature.

[123]  Richard P. Ebstein,et al.  The Oxytocin Receptor (OXTR) Contributes to Prosocial Fund Allocations in the Dictator Game and the Social Value Orientations Task , 2009, PloS one.

[124]  Ilanit Gordon,et al.  Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent–infant contact , 2010, Psychoneuroendocrinology.

[125]  Joseph E LeDoux.  Emotion Circuits in the Brain , 2000 .

[126]  Daniel R. Weinberger,et al.  A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function , 2010, Proceedings of the National Academy of Sciences.

[127]  Shaul Shalvi,et al.  Oxytocin promotes human ethnocentrism , 2011, Proceedings of the National Academy of Sciences.

[128]  William A. Cunningham,et al.  A Functional Magnetic Resonance Imaging Investigation , 2009 .

[129]  Laurie R Santos,et al.  The evolution of intergroup bias: perceptions and attitudes in rhesus macaques. , 2011, Journal of personality and social psychology.

[130]  A. Guastella,et al.  The Role of Oxytocin in Human Affect , 2011 .

[131]  S. Israel,et al.  Intranasal oxytocin modulates EEG mu/alpha and beta rhythms during perception of biological motion , 2010, Psychoneuroendocrinology.

[132]  Szabolcs Kéri,et al.  Oxytocin enhances the perception of biological motion in humans , 2009, Cognitive, affective & behavioral neuroscience.

[133]  Jack L. Vevea,et al.  Beyond the group mind: a quantitative review of the interindividual-intergroup discontinuity effect. , 2003, Psychological bulletin.

[134]  Paul J. Zak,et al.  Monetary sacrifice among strangers is mediated by endogenous oxytocin release after physical contact , 2008 .

[135]  U. Fischbacher,et al.  Oxytocin increases trust in humans , 2005, Nature.